Predictions and errors are distinctly represented across V1 layers

Emily R Thomas; Joost Haarsma; Jessica Nicholson; Daniel Yon; Peter Kok; Clare Press

doi:10.1016/j.cub.2024.04.036

Predictions and errors are distinctly represented across V1 layers

Curr Biol. 2024 May 20;34(10):2265-2271.e4. doi: 10.1016/j.cub.2024.04.036. Epub 2024 May 1.

Authors

Emily R Thomas¹, Joost Haarsma², Jessica Nicholson³, Daniel Yon³, Peter Kok², Clare Press⁴

Affiliations

¹ Neuroscience Institute, New York University Medical Center, 435 East 30(th) Street, New York 10016, USA; Department of Psychological Sciences, Birkbeck, University of London, Malet Street, London WC1E 7HX, UK. Electronic address: emilyrosethomas@outlook.com.
² Wellcome Centre for Human Neuroimaging, Institute of Neurology, University College London, 12 Queen Square, London WC1N 3AR, UK.
³ Department of Psychological Sciences, Birkbeck, University of London, Malet Street, London WC1E 7HX, UK.
⁴ Department of Psychological Sciences, Birkbeck, University of London, Malet Street, London WC1E 7HX, UK; Wellcome Centre for Human Neuroimaging, Institute of Neurology, University College London, 12 Queen Square, London WC1N 3AR, UK; Department of Experimental Psychology, University College London, 26 Bedford Way, London WC1H 0AP, UK. Electronic address: c.press@ucl.ac.uk.

PMID: 38697110
DOI: 10.1016/j.cub.2024.04.036

Abstract

Popular accounts of mind and brain propose that the brain continuously forms predictions about future sensory inputs and combines predictions with inputs to determine what we perceive.¹^,²^,³^,⁴^,⁵^,⁶ Under "predictive processing" schemes, such integration is supported by the hierarchical organization of the cortex, whereby feedback connections communicate predictions from higher-level deep layers to agranular (superficial and deep) lower-level layers.⁷^,⁸^,⁹^,¹⁰ Predictions are compared with input to compute the "prediction error," which is transmitted up the hierarchy from superficial layers of lower cortical regions to the middle layers of higher areas, to update higher-level predictions until errors are reconciled.¹¹^,¹²^,¹³^,¹⁴^,¹⁵ In the primary visual cortex (V1), predictions have thereby been proposed to influence representations in deep layers while error signals may be computed in superficial layers. Despite the framework's popularity, there is little evidence for these functional distinctions because, to our knowledge, unexpected sensory events have not previously been presented in human laminar paradigms to contrast against expected events. To this end, this 7T fMRI study contrasted V1 responses to expected (75% likely) and unexpected (25%) Gabor orientations. Multivariate decoding analyses revealed an interaction between expectation and layer, such that expected events could be decoded with comparable accuracy across layers, while unexpected events could only be decoded in superficial laminae. Although these results are in line with these accounts that have been popular for decades, such distinctions have not previously been demonstrated in humans. We discuss how both prediction and error processes may operate together to shape our unitary perceptual experiences.

Keywords: 7T MRI; action; expectation; laminar fMRI; learning; perception; prediction; sensorimotor prediction.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Adult
Female
Humans
Magnetic Resonance Imaging*
Male
Primary Visual Cortex / physiology
Visual Cortex / physiology
Visual Perception / physiology
Young Adult